The iconic Amanita muscaria. You may have seen some smurfs living in one of these. Public domain; click image for link.

Amanita mushrooms — like all creatures — rot, but most of them can’t rot other things.

The fact that they don’t rot other things is not news to biologists, who have long known that many, if not most, fungi have become professional partners with trees, plants, or algae.

The fact that they can’t rot other things — as reported in July in PLoS ONE — is news, and provides a clue to how symbiotic partnerships can withstand the temptations of leaving and the sometimes dissonant interests of their symbiotic partners.

Amanitas count among their numbers some of the most beautiful and deadly mushrooms on Earth. How would you recognize an Amanita in the woods?

In general, they have sac- or cup-like enclosures called “volvas” from which the young mushrooms emerge. Pieces of this volva often stick to the cap of the mushroom, giving them the characteristic “warts” (or sometimes a little hat) that these fungi are famous for.

Amanitas typically also have a tall, graceful form, often with beautiful striations around the edge of the cap. For a sense of the beauty and diversity in this family, watch this:

The beautiful and lethal "Destroying Angel". This one is likely Amanita bisporigera, since it was observed in the Smoky Mountains. Creative Commons Jason Hollinger; click image for license and link.

The Amanita family also includes some of the best-known tree-partnering fungi on Earth. Many of the mushrooms in this family are mycorrhizae — fungi that coil themselves in and around the roots of trees.

The tree provides them with food it makes topside in return for a vastly improved underground absorptive network. This network, made by the many searching filaments of the fungus, brings much more water and many more minerals to the tree than it would otherwise be able to procure for itself.

Symbioses are widespread on Earth. In fact, they seem to be the rule. In fungi alone, mycorrhizal symbioses seem to have evolved from decaying fungi on at least 11 occasions. Eleven.

But big questions have persisted. How do such living arrangements come to be? Fungi are generally supposed to have evolved from ancestors who were decayers, but mycorrhizal fungi generally lack the ability to decompose. Did the loss precede shacking up with trees, or did it follow it?

Further, what maintains symbioses, how often do symbioses disintegrate, and is it possible for the microbial symbionts to revert to their former lifestyles? For instance, might it still be possible to grow mycorrhizal fungi on leaf litter, or are they really and truly inseparable BFFs with the tree? If so, what keeps them locked in the marriage?

In order to answer those questions, scientists needed a large group of fungi that included both mycorrhizal and saprotrophic species. By studying the pattern of change in the DNA of dozens of different Amanita species, the team from Harvard University and the New York Botanic Garden determined that symbiosis has only arisen once in the Amanitas from decaying ancestors. All the symbiotic Amanitas fell into a single related group, while all the saprotrophic species fell into another, more ancestral group.

The innocuous-looking but deadly Death Cap, Amanita phalloides. Native to Europe, it was likely introduced to America on the roots of imported trees. Creative Commons Archenzo; click image for license and link.

They first checked to see if Amanitas still make the enzymes that free-living decay fungi make to eat leaf litter. They looked specifically at three genes involved in one cellulose digestion pathway (fungi may have several redundant pathways). Cellulose is a major component of plant cell walls and a difficult molecule to digest. Fungi are among the only macro-organisms on Earth that have managed to do so.

The mycorrhizal Amanitas, the scientists found, have lost at least two major enzymes needed to start the break down of cellulose. They retain, however, an enzyme that helps convert small pieces of the polymer cellulose to its monomer glucose — perhaps a sign that the fungi are still content to help themselves to the leftovers of decomposition by sloppy neighboring fungi and microbes, even if they aren’t able to start the feast themselves.

Next, they asked whether Amanitas could actually subsist on dead stuff by testing Amanita‘s ability to grow on sterilized forest litter. Of nine mycorrhizal Amanitas, none could survive on dead plant bits, while all three saprotrophic Amanitas tucked in just fine.

So the mycorrhizal Amanitas tested, at least, have irreversibly lost the genes needed for feeding themselves on their own. Their host trees have become, quite literally, their sugar daddies. What they cannot determine from their data, the scientists wrote, was whether the loss of the ability to digest cellulose preceded or followed the symbiotic living arrangement.

The authors suggest that the latter may be the case via “relaxed selection” — that is, when there’s no cost to offspring to allowing mutations to accumulate in genes whose products are already being provided by a host. I’m speculating here, but there may even be positive selection for individuals who don’t waste their energy making proteins they no longer need.

But not all mycorrhizal fungi are the same. Other mycorrhizal fungi have retained the same cellulose-degrading enzymes that Amanitas seem to have happily lost. The European black truffle and a small, lilac-peachy common forest mushroom called Laccaria bicolor, though both mycorrhizal, retain their versions of the cellulose breakdown enzymes lost by the mycorrhizal Amanitas. The black truffle expresses it extensively in the tree roots where it lives, implying both that it has an important role in symbiosis, and that different mycorrhizal fungi — having evolved seperately many times — have different biochemical relationships with their host trees and different methods that sustain them.

Can symbiotic fungi ever “escape” their lot in life, if conditions warrant? This study suggests that, for Amanitas at least, the answer is no. Still, it’s hard to feel too sorry for them. In making their deal with trees, they surrendered their freedom for some cozy digs and three squares a day. Though symbiosis may be a trap, it’s a gilded cage.

Thanks! Well, I believe a symbiosis (literally “living together”) is an intimate relationship between two *living* organisms. Decayers have a gustatory relationship with a dead organism. So to me, that isn’t symbiosis anymore than your relationship with your salad is a symbiosis. : ) My two cents.

eacastel — The mushroom provides an improved absorptive network of fungal filaments. This network greatly increases the amount of water and minerals the tree can access. I mentioned it briefly in the article but it was probably easy to miss.

Describing the fundamental nature of their symbiosis as nutrition from trees and moisture from fungal filaments was very enlightening! What happens to the relationship when moisture and/or sunlight diminishes? Does the tree stave the fungus when moisture is critical, for example?
Excellent article!

Those are great questions! I’m not sure what the answers are, however. I do know scientists are finding that the relationship between mycorrhizal fungi and their trees is not as straightforwardly hunky-dory as can seem. They each try to maximize what they get out of the relationship! So I imagine it would not be impossible that the tree might regulate what it gives the fungus — or at least attempt to. The fungus has probably evolved many ways of getting around any tricks the tree might throw at it. It can be an uneasy alliance!

Excellent article……it brings back some very good memories when I was a forestry student at the University of Montana back in the early 60′s. I wrote a paper for my forest soils professor on mycorrhiza mostly because it was one of his favorite topics, but I found the subject incredibly interesting and apparently did an excellent job on the paper because the prof gave me the highest grade in the class and made sure all my classmates knew it. This prof was known as the “flunk out” professor for Forestry at U of M and I was pretty proud of myself for the high grade I received. Although I continued school there for 4 years I never did get my degree. The Vietnam war intervened and I also ended up getting involved with being a smokejumper for the Bureau of Land Management in Alaska. That’s a whole another story. I sometimes wish I had chose to study fungi and mycorrhiza as a Botony major instead of the generalized forest management option. Who knows where I could have ended up.

fascinating write-up and extra fascinating and insightful comments this time! love it! jennifer, that extra little analogy about symbiosis and decay was great. i always loved finding the beautiful and mysterious death caps as a kid in the oregon cascade range woods. so interesting that they are not native fungi and yet they are (or seem to be, everywhere?)

hootysdad, sounds like you’ve had some adventures!

and, blueeyedlion: i think what jennifer means is that the bodies of these fungi themselves decay when they die, but they do not facilitate the decay of *other* material. for example, the tree matter they are near/attached to do not decay because of them. do i have it right?

Am I right in thinking that the coal that formed during the corboniferous period was as a result of the inability of fungi to decompose lignin as this only appeared later. This article says that fungi have lost the abilty to decompose cellulose, is this an example of evolution in reverse?

It’s perfect how this Natural science marries to social sciences, since human Nature is what it is. I’ve escaped many times from some Amanita Phalloides types out there.It’s good to have this playbook. Grazie!